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Plants and insect herbivores are two of the most diverse multicellular groups in the world, and both are strongly influenced by interactions with the belowground soil microbiome. Effects of reciprocal rapid evolution on ecological interactions between herbivores and plants have been repeatedly demonstrated, but it is unknown if (and how) the soil microbiome could mediate these eco‐evolutionary processes on a shared host plant. We tested the role of a plant‐beneficial soil bacterium Acidovorax radicis in altering eco‐evolutionary interactions between different aphid genotypes (Sitobion avenae, genotypes Sickte and Fescue) feeding on barley Hordeum vulgare. We measured fecundity, longevity and population growth of two aphid genotypes reared separately or together (population mixture) on three different barley varieties that were inoculated with or without A. radicis. Results showed that across all plant varieties A. radicis increased plant growth and suppressed aphid populations via reduced longevity and fecundity. The strength of effect was dependent on aphid genotype and barley variety, while the direction of effect was altered by aphid population mixture. Using Lotka–Volterra modelling, we demonstrated that while A. radicis inoculation decreased growth rates for both aphid genotypes it increased the competitiveness of one genotype against the other. In general, in the presence of A. radicis, the Fescue aphid genotype became more inhibitory of Sickte aphids, while Sickte aphids facilitated the growth of Fescue aphids. Our work demonstrates that plant rhizosphere microbiomes exert community‐level influences by mediating eco‐evolutionary interactions between herbivores and host plants. By altering competitive interaction outcomes among aphids and thus impacting processes such as rapid evolution, soil microbes contribute to the short‐ and long‐term structure and functioning of terrestrial habitats. [ABSTRACT FROM AUTHOR]